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SYSTEMATIC REVIEW
Servicio de Geriatra, Hospital Universitario Ramn y Cajal, Ctra. Colmenar km 9, 1, 28034 Madrid, Spain
Istituto di Medicina Interna e Geriatria, Universit Cattolica del Sacro Cuore, Rome, Italy
3
Gastroentrologie et Nutrition Clinique, CHU de Nice, Universit de Nice Sophia-Antipolis, Nice, France
4
Universidad Autonoma de Baja California, Tijuana Baja California Mexico, Mexico
5
Department of Human Health Sciences, Kyoto University, Graduate School of Medicine, Kyoto, Japan
6
Unit de Nutrition Humaine, UMR 1019, INRA, Universit Clermont-Ferrand, CHU de Clermont-Ferrand, France
7
Center for Geriatrics and Gerontology, Taipei Veterans General Hospital, Taipei, Taiwan
8
Nutrition, Exercise Physiology, and Sarcopenia Laboratory, Jean Mayer Human Nutrition Research Center on Aging at Tufts
University, Boston, MA, USA
9
Department of Ageing and Health, Guys and St Thomas NHS Foundation Trust, London, UK
10
Dpartement de Rhabilitation et Griatrie, Hpitaux Universitaires de Genve-Suisse, Geneva, Switzerland
11
Institut for Biomedicine of Ageing, University Erlangen-Nrnberg, Erlangen, Germany
12
Institute for Exercise Physiology and Wellness Research, University of Central Florida, Orlando, FL, USA
13
Division of Geriatric Medicine, University of Pittsburgh, Pittsburgh, PA, USA
14
Department of Geriatric Medicine, Inserm U558 Le Centre Hospitalier Universitaire de Toulouse (CHU) Grontople,
Toulouse, France
15
Department of Medicine and Therapeutics, Prince of Wales, Hospital, Chinese University of Hong Kong, Hong Kong SAR,
The Peoples Republic of China
16
Division of Geriatrics, Department of Medicine, University of Verona, Verona, Italy
17
Department of Public Health and Caring Sciences/Clinical Nutrition and Metabolism, Uppsala University, Uppsala, Sweden
2
Abstract
Objective: to examine the clinical evidence reporting the prevalence of sarcopenia and the effect of nutrition and exercise
interventions from studies using the consensus denition of sarcopenia proposed by the European Working Group on
Sarcopenia in Older People (EWGSOP).
Methods: PubMed and Dialog databases were searched ( January 2000October 2013) using pre-dened search terms.
Prevalence studies and intervention studies investigating muscle mass plus strength or function outcome measures using the
EWGSOP denition of sarcopenia, in well-dened populations of adults aged 50 years were selected.
Results: prevalence of sarcopenia was, with regional and age-related variations, 129% in community-dwelling populations, 14
33% in long-term care populations and 10% in the only acute hospital-care population examined. Moderate quality evidence suggests that exercise interventions improve muscle strength and physical performance. The results of nutrition interventions are
equivocal due to the low number of studies and heterogeneous study design. Essential amino acid (EAA) supplements, including
A. J. Cruz-Jentoft et al.
2.5 g of leucine, and -hydroxy -methylbutyric acid (HMB) supplements, show some effects in improving muscle mass and
function parameters. Protein supplements have not shown consistent benets on muscle mass and function.
Conclusion: prevalence of sarcopenia is substantial in most geriatric settings. Well-designed, standardised studies evaluating exercise or nutrition interventions are needed before treatment guidelines can be developed. Physicians should screen for sarcopenia in
both community and geriatric settings, with diagnosis based on muscle mass and function. Supervised resistance exercise is recommended for individuals with sarcopenia. EAA (with leucine) and HMB may improve muscle outcomes.
Keywords: exercise intervention, nutrition intervention, prevalence, age-related, sarcopenia, older people
Methods
Search strategy
Eligibility criteria
Across all three categories, only studies that enrolled participants aged 50 years and older within well-dened populations (such as those in community-dwelling, hospital and
nursing home/geriatric settings) were included. Prevalence
studies were included if sarcopenia had been assessed
according to the EWGSOP denition of sarcopenia, i.e.
based on muscle mass and muscle strength or physical performance [2]. They were excluded if they only used muscle
mass to dene sarcopenia. Nutrition and exercise intervention studies were included if the outcome measures reported
for the interventions included muscle mass and at least one
measure of muscle strength or physical performance, even
when the population studied was not dened as sarcopenic.
If these outcomes were not clearly stated within the study
methodology, the study was excluded. Other criteria used
to exclude studies in each of the three categories are provided
in Supplementary data available in Age and Ageing online,
Appendix S2.
Observational studies were included in the prevalence category, but for the exercise and nutrition intervention categories,
only randomised controlled trials were selected. The ISI group
Introduction
was divided into three subgroups (prevalence, exercise and nutrition). Final papers selected for inclusion in each of the three
categories were agreed upon by each subgroup consensus.
Data synthesis
Results
Overall, 4810 publications were identied (Figure 1). Of
these, 3909 were excluded, leaving 901 publications for potential inclusion ( prevalence: 252; exercise: 175; nutrition:
474). In addition, 11 papers were identied as suitable for inclusion as a result of a short search of PubMed and Dialog
databases to identify articles published in the period May
October 2013.
Eighteen prevalence, 7 exercise and 12 nutrition papers
were nally chosen by the working group members for inclusion within this review (Figure 1).
Estimates of prevalence
Reference
Country
M/F, n
Assessment method
Muscle mass
Muscle strength
Physical
performance
Sarcopenia prevalence, %
Total
Male
Female
.................................................................................................................
Community-dwelling populations
Abellan van Kan et al. [5]
Jan 1992Jan 1994
France
0/3025
DEXA
HS
GS
80.51 (3.9)
[75]
82.2 (1.4)
[8085]
85.8 (4.9)
73.7 (5.6)
5.2
5.2
21.8
25.7
19.8
29.1
7.8a
16.6b
12.5
27.1
10.8a
14.9b
14.6
30.1
3.7a
19.0b
12.4
4.1
S: 5
SS: 0
S: 7
SS: 0
(A): 6.8
(B): 7.8
4.6
7.9
0.9
0.9
24.2
24.2
11.3
10.7
S: 3.7
SS: 0
10.2
2.6
6.7
21.8
22.1
All: 14.3
5064: 12.7
65: 17.4
Oct 2003
Italy
66/131
MAMC
HS
GS
Oct 2003
Italy
Taiwan
118/236
223/163
MAMC
DXA
HS
HS, KE, PEF
Belgium
103/185
BIA
HS
GS
SPPB, GS, TUG,
or SCPT
mSPPB, GS
124/195
DEXA
GS
USA (African
Americans)
Canada
84.8 (3.6)
[>80]
59.2 (4.4)
42/43
BIA
HS
GS
75.2 (5.7)
6.0
USA
1426/1502
DEXA
HS
GS
S: 5
UKc
Cohort A: 103/0
Cohort B: 765/1022
DEXA, SFT
HS
GS, TUG,
chair-rise time
Finland
0/409
DEXA
HS
Japan
0/533
DEXA
HS, LEP
MayJun 2007,
2008, 2009
Japan
364/794
BIA
HS
GS
Belgium, UK
679/0
DEXA
HS, KE
GS
20042006
Italy
250/288
BIA
HS
GS
Japan
568/1314
BIA
HS
GS
F: 73.5 (2.88)
M: 73.8 (2.85)
Total: [7079]
(A): 72.5 (2.5)
(B): M, 67.0 (2.6);
F, 67.1 (2.6)
74.2 (3.0)
[7080]
<39: 11.4%
<49: 21.2%
<59: 25.9%
<69: 29.8%
<85: 11.6%
[3084]
M: 74.4 (6.4)
F: 73.9 (6.3)
[65]
59.6 (10.7)
[4079]
77.1 (5.5)
[6597]
74.9 (5.5)
[6589]
Institutional dwelling
Bastiaanse et al. [20]
Netherlands
450/434
CC
HS
GS
5059: 46.5%
6069: 35.2%
7079: 16.2%
80: 2.1%
[50]
A. J. Cruz-Jentoft et al.
ALM, appendicular lean mass; BIA, bioelectrical impedance analysis; CC, calf circumference; DEXA, dual-energy X-ray absorptiometry; F, female; GS, gait speed; HS, hand-grip strength using a dynamometer; KE, knee
extensor; LEP, leg extension power; M, male; MAMC, mid-arm muscle circumference; PEF, peak expiratory flow; S, sarcopenia; SCPT, stair-climb power test; SD, standard deviation; SFT, skin-fold thickness; (m)SPPB,
(modified) standard physical performance battery; SS, severe sarcopenia; TUG, timed-up-and-go; VO2max, maximal oxygen uptake.
a
By relative appendicular skeletal muscle index.
b
By percentage skeletal muscle index.
c
Consists of two cohorts (Cohort A: detailed data were collected. Cohort B: same data were collected, but no DEXA).
*P < 0.001 versus females.
10.2
[65]
MAMC
UK
Acute hospital care
Gariballa and Alessa [22]
227/205
HS
84.1 (4.8)
[70]
HS
BIA
31/91
Italy
AugSep 2010
Landi et al. [21]
There were seven moderate quality (PEDro score: 46) intervention studies that investigated the effect of exercise on
muscle parameters in different populations aged 6095 years
(Table 2) [2329]. The impact of exercise on sarcopenia was
assessed using muscle mass and muscle strength or power
measures in all studies [2329]; assessment of physical performance (chair rise [24], 12-min walk [25], stair climbing
[29] or timed up and go [27, 28]) was carried out in ve of
seven studies (Table 2).
Resistance training interventions
Three additional studies explored compound exercise interventions (with different blends of aerobic, resistance, exibility and/or balance training), which were performed for 318
months [2628]. A high-intensity multipurpose exercise programme over 18 months improved muscle mass, muscle
strength and physical performance versus control (wellbeing)
in a study in 246 women [27]. In two mixed-gender studies
GS
32.8
67.7
20.8*
Reference
Population
Number
studied
(M/F)
Age, years
Mean (SD)
[Range]
91
83 (4)
MM (DEXA), MS (KE)
57 (7/50)
83
98 (36/62)
70
18
Intervention
Description
Duration
(months)
PEDro
score
Outcomes measured
Main results
.................................................................................................................
Binder et al.
[23]
Frail, community-dwelling
Suetta et al.
[29]
Frail, post-operative
36 (18/18)
elective hip replacement
[6086]
MM (US), MS (quadriceps), PP
(stair climbing)
Goodpaster
et al. [26]
Sedentary,
community-dwelling
42 (11/31)
[7089]
12
246 (0/246)
69.1 [6580]
18
MM (DEXA), MS (isometric
leg extension), PP (timed up
and go)
Rydwik et al.
[28]
96 (38/58)
>75
Frail, community-dwelling
BW, body weight; CON, control; CT, computerised tomography; DEXA, dual-energy X-ray absorptiometry; ES, electrical stimulation; F, female; FFM, free-fat mass; FM, fat mass; KE, knee extension; M, male; min, minute;
MM, muscle mass; MP, muscle power; MS, muscle strength; RET, resistance exercise training; PA, physical activity; PLA, placebo; PP, physical performance; SD, standard deviation; SUPP, nutritional supplement;
US, ultrasound.
A. J. Cruz-Jentoft et al.
6
Table 2. Summary of the effect of exercise on sarcopenia in randomised, controlled studies meeting the inclusion criteria
Nutrition interventions
Protein supplements
The only study examining the effect of fatty acid supplementation (-linolenic acid) on muscle parameters (PEDro score:
10), in 51 older adults undergoing resistance training for 12
weeks, showed no effect of the supplementation on muscle
mass or muscle strength versus placebo [31].
Discussion
Sarcopenia is an independent risk factor for adverse outcomes, including difculties in instrumental and basic ADL
[6, 10, 16, 20, 21], osteoporosis [17], falls [21], hospital length
of stay and re-admission [22] and death [6]. This underscores
the importance of understanding the true prevalence of sarcopenia and effective preventative strategies.
Prevalence
Reference
Population
Number studied
(M/F)
PEDro
Score
Intervention (duration)
Outcomes measured
Main results
.................................................................................................................
Bonnefoy et al. [24]
57 (7/50)
83
Community-dwelling
98 (36/62)
[70]
Sedentary,
community-dwelling
80 (33/47)
[7085]
10
Frail,
community-dwelling
62 (21/41)
10
Frail,
community-dwelling
65 (29/36)
Healthy individuals
14 (0/14)
Community-dwelling
155 (0/155)
PLA: 79 (6)
Protein: 78 (9)
[65]
PLA: 81 (1 SEM)
Protein 78 (1
SEM)
65
All: 68 (2)
PLA: 69 (3)
Supplement: 67 (1)
79 (2.9)
[75]
Community-dwelling
57 (0/57)
Healthy individuals on
bed rest
19 (4/15)
76.7
[6290]
10
HMB; PLA
Bed rest (10 days) + rehabilitation
(8 weeks)
A. J. Cruz-Jentoft et al.
8
Table 3. Summary of the effect of nutrition on sarcopenia in randomised, controlled studies meeting the inclusion criteria
ALA, -linolenic acid; ARG, arginine; BIA, bioelectrical impedance analysis; CON, controls; CT, computerised tomography; DEXA, dual X-ray absorptiometry; EAA, essential amino acid; F, female; FFM, fat-free mass; HE,
health education; HIS, histidine; HMB, -hydroxy -methylbutyrate; ILE, isoleucine; HS, hand-grip strength; KE, knee extension; LE, leg extension; LEU, leucine; LYS, lysine; M, male; min, minute; MET, methionine; MM,
muscle mass; MP, muscle power; MS, muscle strength; NS, not significant; PHE, phenylalanine; PLA, placebo; PP, physical performance; RET, resistance exercise training; SD, standard deviation; SPPB, standard physical
performance battery; SUPP, nutritional supplement; THR, threonine; VAL, valine; WPS, whey protein supplement.
70 (1)
Community-dwelling
Vukovich et al. [39]
31 (15/16)
10
MM (DEXA), MS (isokinetic
leg strength, HS), PP
(get up and go)
Phase I: HMB; PLA (24 weeks)
Phase II: PLA + RET; HMB + RET
(24 weeks)
9
73 (1 SEM)
[65]
98 (49/49)
Community-dwelling
Stout et al. [36]
Exercise intervention
A. J. Cruz-Jentoft et al.
Nutrition intervention
Further studies are needed to determine the effect of different nutrition interventions on muscle mass and function
using robust, multi-centre and standardised approaches
with single or complex nutrition interventions and clinically
relevant outcomes (muscle strength, physical performance).
Studies using four arms (exercise, nutrition, both or none)
should also be conducted. The choice of exercise and nutrition interventions should be based on the singular effect of
each intervention.
Outcome measures for such studies should not differ from
those used for individual components, and reporting
should allow for individual group comparisons to also
evaluate the role of each component.
Timing of nutrition intervention before or after exercise
should be explored in clinical trials comparing different times
of administration, as basic studies suggest there may be timeassociated differences in the effect of nutrition intervention
over exercise.
Baseline nutritional status and physical frailty of the population should be considered when doing nutrition intervention studies.
Key points
The reported prevalence of sarcopenia in the community is
up to 33%, with higher prevalence in long-term and acute
care settings.
This underscores the importance of preventative and clinical
management strategies for managing sarcopenia.
While further research is needed on interventions, we
provide recommendations for clinical practice.
The ISI included representatives of the European Working
Group on Sarcopenia in Older People (EWGSOP), the
International Working Group on Sarcopenia (IWGS) and
international experts.
Practice recommendations
10
Conflicts of interest
Abbott had no role in the choice of members of the group,
but had the right to have an observer member at the meetings. Members of the Working Group received no salary or
other incomes from the European Union Geriatric medicine
Society (EUGMS), Abbott Nutrition (AN) or any other
Although nutrition intervention is considered one of the mainstays of intervention in sarcopenia, much of the evidence is
based on short-term protein synthesis studies, and large clinical
trials are still lacking. Our review has failed to show a consistent
effect of protein supplementation, although the number of
studies found using our strict selection criteria was very low.
EAAs (with 2.5 g of leucine) and HMB seem to have some
effects on muscle mass and muscle function that need to be
conrmed in larger trials. Vitamin D studies were evaluated as
part of the review process; while some epidemiological studies
link vitamin D levels with muscle parameters, there were no
intervention studies meeting the criteria for inclusion in this
review. Similarly, there is a large literature on the effects of
omega 3-fatty acids on muscle parameters, especially in cachexia,
but only one negative study was found in this review [31].
Interventions that evaluated the combined effects of exercise
and nutrition sometimes suggested a potential additive effect, although this needs further research. However, solid evidence on
which to base recommendations for patients with sarcopenia is
not available.
Funding
This work was supported by an unrestricted educational
grant provided by AN to EUGMS. This grant was used for
operational activities including two meetings of the Working
Group.
Supplementary data
References
The full list of references is available on Supplementary data
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